Abstract
In this study, the feasibility and applicability of marine algal biomass Saccharina (Laminaria) japonica as a sole substrate for the production of pigments by Talaromyces amestolkiae GT11 in submerged fermentation was evaluated. Results indicated that the fungus T. amestolkiae GT11 produced the highest amount of extracellular yellow (444.83 ± 22) and red (200.94 ± 12), and intracellular yellow (362.28 ± 34) and red (193.87 ± 10) pigments, utilizing 1% (w/v) of S. japonica powder at an initial pH of 5 and 30°C, as compared to other physiochemical parameters tested. The pH and thermostability analysis results demonstrated that even after 5 h of incubation the pigment was found to be highly stable at pH 6 and 40 ~ 60°C with 98% and 90.56 ~ 84.69% of residual absorbance, respectively. Apart from the application of pigment as a natural colorant instead of synthetic one in biotechnology industry, the fermented substrate itself can be exploited as food and feed with enhanced nutrient content, improved protein quality and fiber digestibility, etc. However, further studies concerning the safety and functional properties of the pigment and fermented substrate are required. Furthermore, this study provides the evidences about the biological method of making easily fermentable biomass for biorefiners or other metabolite production.
Similar content being viewed by others
References
Méndez, A., C. Pérez, J. C. Montañéz, G. Martínez, and C. N. Aguilar (2011) Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J. Zhejiang. Univ-SCI. B Biomed. Biotechnol. 12: 961–968.
Gunasekaran, S. and R. Poorniammal (2008) Optimization of fermentation conditions for red pigment production from Penicillium sp. under submerged cultivation. Afr. J. Biotechnol. 7: 1894–1898.
Dufossé, L., P. Galaup, A. Yaron, S. M. Arad, P. Blanc, K. N. C. Murthy, and G. A. Ravishankar (2005) Microorganisms and microalgae as sources of pigments for food use: A scientific oddity or an industrial reality? Trends Food Sci. Technol. 16: 389–406.
Blanc, P. J., M. O. Loret, A. L. Santerre, A. Pareilleux, D. Prome, J. C. Prome, J. P. Laussac, and G. Goma (1994) Pigments of Monascus. J. Food Sci. 59: 862–865.
Tseng, Y. Y., M. T. Chen, and C. F. Lin (2000) Growth, pigment production and protease activity of Monascus purpureus as affected by salt, sodium nitrite, polyphosphate and various sugars. J. Appl. Microbiol. 88: 31–37.
Carvalho, J. C., A. Pandey, S. Babitha, and C. R. Soccol (2003) Production of Monascus biopigments: an overview. Agro. Food Ind. Hi-Tech. 14: 37–42.
Engstrom, G. W., R. E. Stenkamp, D. J. McDorman, and L. H. Jensen (1982) Spectral identification, X-ray structure determination, and iron chelating capability of erythroglaucin, a red pigment from Aspergillus ruber. J. Agric. Food Chem. 30: 304–307.
Méndez-Zavala, A., J. C. Contreras-Esquivel, F. Lara-Victoriano, R. Rodríguez-Herrera, and C. N. Aguilar (2007) Fungal production of a red pigment using a xerophilic strain of Penicillium purpurogenum GH2. Rev. Mex. Ing. Quím. 6: 267–273.
Mapari, S. A. S., K. F. Nielsen, T. O. Larsen, J. C. Frisvad, A. S. Meyer, and U. Thrane (2005) Exploring fungal biodiversity for the production of water soluble pigments as potential natural food colorants. Curr. Opin. Biotechnol. 16: 231–238.
Mapari, S. A. S., A. S. Meyer, U. Thrane, and J. C. Frisvad (2009) Identification of potentially safe promising fungal cell factories for the production of polyketide natural food colorants using chemotaxonomic rationale. Microb. Cell Fact. 8: 25.
Ogihara, J. and K. Oishi (2002) Effect of ammonium nitrate on the production of PP-V and monascorubrin homologues by Penicillium sp. AZ. J. Biosci. Bioeng. 93: 54–59.
Samson, R. A., N. Yilmaz, J. Houbraken, H. Spierenburg, K. A. Seifert, S. W. Peterson, J. Varga, and J. C. Frisvad (2011) Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium. Stud. Mycol. 70: 159–183.
Yilmaz, N., J. Houbraken, E. S. Hoekstra, J. C. Frisvad, C. M. Visagie, and R. A. Samson (2012) Delimitation and characterization of Talaromyces purpurogenus and related species. Persoonia. 29: 39–54.
Babitha, S., C. R. Soccol, and A. Pandey (2006) Jackfruit seed-a novel substrate for the production of Monascus pigments through solid-state fermentation. Food Technol. Biotechnol. 44: 465–471.
Wei, N., J. Quarterman, and Y. S. Jin (2013) Marine macroalgae: An untapped resource for producing fuels and chemicals. Trends Biotechnol. 31: 70–77.
Holdt, S. L. and S. Kraan (2011) Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 23: 543–597.
Bartsch, I., C. Wiencke, K. Bischof, C. M. Buchholz, H. Buck, A. Eggert, P. Feuerpfeil, D. Hanelt, S. Jacobsen, R. Karez, U. Karsten, M. Molis, M. Y. Roleda, H. Schubert, R. Schumann, K. Valentin, F. Weinberger, and J. Wiese (2008) The genus Laminaria sensulato: recent insights and developments. Eur. J. Phycol. 43: 1–86.
Jung, K. A., S. R. Lim, Y. Kim, and J. M. Park (2013) Potential of macroalgae as feed stocks for biorefinery. Bioresour. Technol. 135: 182–190.
Chae, H. R. and S. K. Kim (2013) Optimization of pretreatment conditions and use of a two stage fermentation process for the production of ethanol from seaweed, Saccharina japonica. Biotechnol. Bioproc. Eng. 18: 715–720.
Gupta, S., N. Abu-Ghannam, and A. G. M. Scannell (2011) Growth and Kinetics of Lactobacillus plantarum in the fermentation of edible Irish brown seaweeds. Food Bioprod. Proc. 89: 346–355.
General, T., H. J. Kim, B. Prasad, H. T. A. Ngo, N. Vadakedath, and M. G. Cho (2013) Fungal utilization of a known and safe macroalga for pigment production using solid-state fermentation. J. Appl. Phycol. doi: 10.1007/s10811-013-0168-3.
Sakurai, Y., T. H. Lee, and H. Shiota (1977) On the convenient method for glucosamine estimation in Koji. Agric. Biol. Chem. 41: 619–624.
Nielsen, S. S. (2003) Phenol-sulfuric acid method for total carbohydrates. Food Analysis Laboratory Manual. pp. 39–44. Indiana, Kluwer Academic/Plenum Publisher.
Kang, B., X. Zhang, Z. Wu, H. Qi, and Z. Wang (2003) Effect of pH and nonionic surfactant on profile on intracellular and extracellular Monascus pigments. Proc. Biochem. 48: 759–767.
Hamano, P. S., S. F. B. Orozco, and B. V. Kilikian (2005) Concentration determination of extracellular and intracellular red pigments produced by Monascus sp. Braz. Arch. Biol. Technol. 48: 43–49.
Evans, P. J. and H. Y. Wang (1984) Pigment production from immobilized Monascus sp. utilizing polymeric resin adsorption. Appl. Environ. Microbiol. 47: 1323–1326.
Bühler, R. M. M., A. C. Dutra, F. Vendruscolo, D. E. Moritz, and J. L. Ninow (2013) Monascus pigment production in bioreactor using a co-product of biodiesel as substrate. Ciênc. Tecnol. Aliment. 33: 9–13.
Leesing, R. and P. Karraphan (2011) Kinetic growth of the isolated oleaginous yeast for microbial lipid production. Afr. J. Biotechnol. 10: 13867–13877.
Santos-Edinum, V. C., I. C. Roberto, M. F. Simas Teixeira, and A. Pessoa (2013) Improving of red colorants production in submerged culture and the effect of different parameters in their stability. Biotechnol. Prog. 29: 778–7785.
Sánchez, Ã. J. and C. A. Cardona (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour. Technol. 99: 5270–5295.
Yongsmith, B., V. Kitprechavanich, L. Chitrandon, C. Chaisrisook, N. Budda (2000) Color mutants of Monascus sp. KB9 and their comparative glucoamylase on rice solid culture. J. Mol. Catal. B: Enzym. 10: 263–272.
Velmurugan, P., H. Hur, V. Balachandar, S. Kamala-Kannan, K. J. Lee, S. M. Lee, J. C. Chae, P. J. Shea, and B. T. Oh (2011) Monascus pigment production by solid-state fermentation with corn cob substrate. J. Biosci. Bio. Eng. 112: 590–594.
Babitha, S., C. R. Soccol, and A. Pandey (2007) Solid-state fermentation for the production of Monascus pigments from jackfruit seed. Bioresour. Technol. 98: 1554–1560.
Johns, M. R. and D. M. Stuart (1991) Production of pigments by Monascus purpureus in solid culture. J. Ind. Microbiol. 8: 23–28.
Gombert, A. K., A. L. Pinto, L. R. Castilho, and D. M. G. Freire (1999) Lipase production by Penicillium restrictum in solid-state fermentation using babassu oil cake as substrate. Proc. Biochem. 35: 85–90.
Raimbault, M. (1998) General and microbiological aspects of solid substrate fermentation. Electro. J. Biotechnol. 1: 1–20.
Orozco, S. F. and B. V. Kilikian (2008) Effect of pH on citrinin and red pigments production by Monascus purpureus CCT3802. World J. Microbiol. Biotechnol. 24: 263–268.
Mapari, S. A. S., A. S. Meyer, and U. Thrane (2008) Evaluation of Epicoccum nigrum for growth, morphology and production of natural colorants in liquid media and on solid rice medium. Biotechnol. Lett. 30: 2183–2190.
Gao, L., H. S. Man, Z. L. Xing, and C. S. Yong (2007) Effects of carbon concentration and carbon to nitrogen ratio on the growth and sporulation of several biocontrol of fungi. Mycol. Res. 111: 87–92.
Feng, M., Y. Shao, and F. Chen (2012) Monascus pigments. Appl. Microbiol. Biotechnol. 96: 1421–1440.
Lin, T. F. and A. L. Demain (1991) Effect of nutrition of Monascus sp. on formation of red pigments. Appl. Microbiol. Biotechnol. 36: 70–75.
Jespersen, L., L. D. Stromdahl, K. Olsen, and L. H. Skibsted (2005) Heat and light stability of three natural blue colorants for use in confectionery and beverages. Eur. Food. Res. Technol. 220: 261–266.
Silveria, S. T., D. L. Daroit, V. Sant Anna, and A. Brandelli (2011) Stability modeling of red pigment produced by Monascus purpureus in submerged cultivations with sugarcane bagasse. Food Bioproc. Technol. doi:10.1007/s11947-011-0710-8.
Mapari, S. A. S., A. S. Meyer, and U. Thrane (2009) Photo stability of natural orange-red and yellow pigments in liquid food model systems. J. Agric. Food. Chem. 57: 6253–6261.
Carvalho, J. C., B. O. Oishi, A. Pandey, and C. R. Soccol (2005) Biopigments from Monascus: Strain selection, citrinin production and color stability. Braz. Arch. Bio. Technol. 48: 885–894.
Nimnoi, P. and S. Lumyong (2011) Improving solid-state fermentation of Monascus purpureus on agricultural products for pigment production. Food Bioproc. Technol. 4: 1384–1390.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
General, T., Prasad, B., Kim, HJ. et al. Saccharina japonica, a potential feedstock for pigment production using submerged fermentation. Biotechnol Bioproc E 19, 711–719 (2014). https://doi.org/10.1007/s12257-013-0709-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12257-013-0709-2